Iron homeostasis in the absence of ferricrocin and its consequences in fungal development and insect virulence in Beauveria bassiana

Abstract The putative ferricrocin synthetase gene ferS in the fungal entomopathogen Beauveria bassiana BCC 2660 was identified and characterized. The 14,445-bp ferS encodes a multimodular nonribosomal siderophore synthetase tightly clustered with Fusarium graminearum ferricrocin synthetase. Function...

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Main Authors: Jiraporn Jirakkakul, Nuchnudda Wichienchote, Somsak Likhitrattanapisal, Supawadee Ingsriswang, Thippawan Yoocha, Sithichoke Tangphatsornruang, Rudsamee Wasuwan, Supapon Cheevadhanarak, Morakot Tanticharoen, Alongkorn Amnuaykanjanasin
Format: Article
Language:English
Published: Nature Publishing Group 2021-10-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-99030-4
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spelling doaj-f240bac2c5114a34a2f0d137cacb027e2021-10-10T11:26:01ZengNature Publishing GroupScientific Reports2045-23222021-10-0111111510.1038/s41598-021-99030-4Iron homeostasis in the absence of ferricrocin and its consequences in fungal development and insect virulence in Beauveria bassianaJiraporn Jirakkakul0Nuchnudda Wichienchote1Somsak Likhitrattanapisal2Supawadee Ingsriswang3Thippawan Yoocha4Sithichoke Tangphatsornruang5Rudsamee Wasuwan6Supapon Cheevadhanarak7Morakot Tanticharoen8Alongkorn Amnuaykanjanasin9Pilot Plant Development and Training Institute, King Mongkut’s University of Technology ThonburiNational Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development AgencyNational Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development AgencyNational Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development AgencyNational Omics Center, National Science and Technology Development AgencyNational Omics Center, National Science and Technology Development AgencyNational Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development AgencyPilot Plant Development and Training Institute, King Mongkut’s University of Technology ThonburiPilot Plant Development and Training Institute, King Mongkut’s University of Technology ThonburiNational Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development AgencyAbstract The putative ferricrocin synthetase gene ferS in the fungal entomopathogen Beauveria bassiana BCC 2660 was identified and characterized. The 14,445-bp ferS encodes a multimodular nonribosomal siderophore synthetase tightly clustered with Fusarium graminearum ferricrocin synthetase. Functional analysis of this gene was performed by disruption with the bar cassette. ΔferS mutants were verified by Southern and PCR analyses. HPLC and TLC analyses of crude extracts indicated that biosynthesis of ferricrocin was abolished in ΔferS. Insect bioassays surprisingly indicated that ΔferS killed the Spodoptera exigua larvae faster (LT50 59 h) than wild type (66 h). Growth and developmental assays of the mutant and wild type demonstrated that ΔferS had a significant increase in germination under iron depletion and radial growth and a decrease in conidiation. Mitotracker staining showed that the mitochondrial activity was enriched in ΔferS under both iron excess and iron depletion. Comparative transcriptomes between wild type and ΔferS indicated that the mutant was increased in the expression of eight cytochrome P450 genes and those in iron homeostasis, ferroptosis, oxidative stress response, ergosterol biosynthesis, and TCA cycle, compared to wild type. Our data suggested that ΔferS sensed the iron excess and the oxidative stress and, in turn, was up-regulated in the antioxidant-related genes and those in ergosterol biosynthesis and TCA cycle. These increased biological pathways help ΔferS grow and germinate faster than the wild type and caused higher insect mortality than the wild type in the early phase of infection.https://doi.org/10.1038/s41598-021-99030-4
collection DOAJ
language English
format Article
sources DOAJ
author Jiraporn Jirakkakul
Nuchnudda Wichienchote
Somsak Likhitrattanapisal
Supawadee Ingsriswang
Thippawan Yoocha
Sithichoke Tangphatsornruang
Rudsamee Wasuwan
Supapon Cheevadhanarak
Morakot Tanticharoen
Alongkorn Amnuaykanjanasin
spellingShingle Jiraporn Jirakkakul
Nuchnudda Wichienchote
Somsak Likhitrattanapisal
Supawadee Ingsriswang
Thippawan Yoocha
Sithichoke Tangphatsornruang
Rudsamee Wasuwan
Supapon Cheevadhanarak
Morakot Tanticharoen
Alongkorn Amnuaykanjanasin
Iron homeostasis in the absence of ferricrocin and its consequences in fungal development and insect virulence in Beauveria bassiana
Scientific Reports
author_facet Jiraporn Jirakkakul
Nuchnudda Wichienchote
Somsak Likhitrattanapisal
Supawadee Ingsriswang
Thippawan Yoocha
Sithichoke Tangphatsornruang
Rudsamee Wasuwan
Supapon Cheevadhanarak
Morakot Tanticharoen
Alongkorn Amnuaykanjanasin
author_sort Jiraporn Jirakkakul
title Iron homeostasis in the absence of ferricrocin and its consequences in fungal development and insect virulence in Beauveria bassiana
title_short Iron homeostasis in the absence of ferricrocin and its consequences in fungal development and insect virulence in Beauveria bassiana
title_full Iron homeostasis in the absence of ferricrocin and its consequences in fungal development and insect virulence in Beauveria bassiana
title_fullStr Iron homeostasis in the absence of ferricrocin and its consequences in fungal development and insect virulence in Beauveria bassiana
title_full_unstemmed Iron homeostasis in the absence of ferricrocin and its consequences in fungal development and insect virulence in Beauveria bassiana
title_sort iron homeostasis in the absence of ferricrocin and its consequences in fungal development and insect virulence in beauveria bassiana
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-10-01
description Abstract The putative ferricrocin synthetase gene ferS in the fungal entomopathogen Beauveria bassiana BCC 2660 was identified and characterized. The 14,445-bp ferS encodes a multimodular nonribosomal siderophore synthetase tightly clustered with Fusarium graminearum ferricrocin synthetase. Functional analysis of this gene was performed by disruption with the bar cassette. ΔferS mutants were verified by Southern and PCR analyses. HPLC and TLC analyses of crude extracts indicated that biosynthesis of ferricrocin was abolished in ΔferS. Insect bioassays surprisingly indicated that ΔferS killed the Spodoptera exigua larvae faster (LT50 59 h) than wild type (66 h). Growth and developmental assays of the mutant and wild type demonstrated that ΔferS had a significant increase in germination under iron depletion and radial growth and a decrease in conidiation. Mitotracker staining showed that the mitochondrial activity was enriched in ΔferS under both iron excess and iron depletion. Comparative transcriptomes between wild type and ΔferS indicated that the mutant was increased in the expression of eight cytochrome P450 genes and those in iron homeostasis, ferroptosis, oxidative stress response, ergosterol biosynthesis, and TCA cycle, compared to wild type. Our data suggested that ΔferS sensed the iron excess and the oxidative stress and, in turn, was up-regulated in the antioxidant-related genes and those in ergosterol biosynthesis and TCA cycle. These increased biological pathways help ΔferS grow and germinate faster than the wild type and caused higher insect mortality than the wild type in the early phase of infection.
url https://doi.org/10.1038/s41598-021-99030-4
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